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Patterns of Evolution in the Feeding Mechanism of Actinopterygian Fishes1

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Patterns of Evolution in the Feeding Mechanism of Actinopterygian Fishes1 AMER. ZOOL., 22:275-285 (1982) Patterns of Evolution in the Feeding Mechanism of Actinopterygian Fishes1 GEORGE V. LAUDER Department of Anatomy, University of Chicago, Chicago, Illinois 60637 SYNOPSIS. Structural and functional patterns in the evolution of the actinopterygian feeding mechanism are discussed in the context of the major monophyletic lineages of ray-finned fishes. A tripartite adductor mandibulae contained in a maxillary-palatoquad- rate chamber and a single mechanism of mandibular depression mediated by the obliquus inferioris, sternohyoideus, and hyoid apparatus are primitive features of the Actinopte- rygii. Halecostome fishes are characterized by having an additional mechanism of man- dibular depression, the levator operculi—opercular series coupling, and a maxilla which swings anteriorly during prey capture. These innovations provide the basis for feeding by inertial suction which is the dominant mode of prey capture throughout the haleco- stome radiation. A remarkably consistent kinematic profile occurs in all suction-feeding halecostomes. Teleost fishes possess a number of specializations in the front jaws including a geniohyoideus muscle, loss of the primitive suborbital adductor component, and a mobile premaxilla. Structural innovations in teleost pharyngeal jaws include fusion of the dermal tooth plates with endoskeletal gill arch elements, the occurrence of a pharyngeal retractor muscle, and a shift in the origin of the pharyngohyoideus. These specializations relate to increased functional versatility of the pharyngeal jaw apparatus as demonstrated by an electromyographic study of pharyngeal muscle activity in Esox and Ambloplites. The major feature of the evolution of the actinopterygian feeding mechanism is the increase in structural complexity in both the pharyngeal and front jaws. Structural diversification is a function of the number of independent biomechanical pathways governing movement. INTRODUCTION and function in fishes and in the proposal The evolution of the feeding mechanism and testing of functional explanations for in ray-finned fishes (Actinopterygii) pro- structure (Alexander, 1966, 1967, 1970; vides perhaps the best documented ex- Anker, 1974; Lauder, 1979; Liem, 1970; ample in the Vertebrata of change in a Osse, 1969). Functional analysis has be- structurally and functionally complex sys- come increasingly sophisticated and tech- tem. In the twenty years since the last re- niques such as high-speed cinematography view of the evolution of the feeding mech- (Elshoud-Oldenhave and Osse, 1976; Gro- anism in ray-finned fishes (Schaeffer and becker and Pietsch, 1979; Nyberg, 1971), Rosen, 1961), knowledge of both the his- electromyography (Ballintijn et al., 1972; torical pattern of diversification and the Lauder, 1980a; Liem, 1973; Liem and relation between structure and function Osse, 1975; Vandewalle, 1979), strain has increased tremendously. Phylogenetic gauges (Lauder and Lanyon, 1980), and analyses of actinopterygian evolutionary pressure transducers (Alexander, 1970; patterns have provided an excellent base- Lauder, 19806, c; Osse and Muller, 1981) line of information on the historical se- have largely obviated the need to base quence of structural change (Greenwood functional considerations on manipula- et al., 1966, 1973; Patterson, 1977, 1982; tions of preserved or freshly dead speci- Patterson and Rosen, 1977; Rosen, 1982), mens. As a result, many hypotheses about and as the discipline of experimental func- the functional significance of morpholog- tional morphology has developed, a cor- ical features in the actinopterygian skull responding increase has occurred in the have been tested, and many previously un- analysis of the relationship between form suspected relationships have emerged. In this paper, I will focus on structural and functional specializations in the evo- 1 From the Symposium on Evolutionary Morphology lution of the actinopterygian feeding of the Actinopterygian Fishes presented at the Annual Meeting of the American Society of Zoologists, 27- mechanism as they are reflected in nested 30 December 1980, at Seattle, Washington. sets of monophyletic lineages. I will em- 275 276 GEORGE V. LAUDER MX BM HVOID FIG. 2. Reconstruction of the superficial lateral (A) and ventral (B) cranial musculature in the paleonis- ciform fish Moythomasia nilida Gross. Osteological ele- ments modified after Jessen (1968). The anterior branchiostegal rays have been removed in the ventral view to show the reconstructed throat musculature, and the maxilla in the lateral view has been partially removed to reveal the adductor musculature. The paired sternohyoideus muscles lie deep to the inter- mandibularis posterior and interhyoideus and are not FIG. 1. Structural network in the head of a primitive visible in this view. This reconstruction results from actinopterygian (A), a primitive halecostome (B), and deducing the most parsimonious primitive arrange- a percomorph (C) to show the biomechanical path- ment of adductor muscle character states in living ways governing mouth opening, suction feeding, and actinopterygians. Abbreviations: AMa, anterior (sub- jaw protrusion functions. Homologous biomechanical orbital) division of the adductor mandibulae; AMm, pathways are similarly numbered. Note the increase medial adductor division; AMp, posterolateral ad- in complexity of the structural network in actinop- ductor division; BM, branchiomandibularis muscle; terygian evolution. Only the function of jaw protru- CL, cleithrum; CLAV, clavicle; EP, epaxialis; IH, sion is shown in (C); the primitive functions of mouth interhyoideus; IMp, intermandibularis posterior opening and suction feeding are omitted for clarity. muscle; IO, infraorbital bone; MD, mandible; MX, Solid rectangles = bony elements; dashed rectan- maxilla; OBI, obliquus inferioris; OBS, obliquus gles = ligaments; parallelograms = muscles. Arrows superioris; OP, operculum; POP, preoperculum. run from the muscle to the bone of insertion; double- headed arrows indicate ligamentous connections be- tween bony elements. Three dimensional rectangles indicate major functions which are realized (r, ar- adductor operculi muscle; EM, epaxial muscles; HY, rows) by the biomechanical couplings indicated. This hypaxial (obliquus inferioris) musculature; IHL, in- figure is not the same as the diagrams depicting the teroperculohyoid ligament; IML, interoperculoman- pattern of interrelationships and functional influ- dibular ligament; LAP, levator arcus palatini muscle; ences (see Dullemeijer, 1974, Fig. 62). Abbreviations: LOP, levator operculi muscle; MHL, mandibulohyoid AMI, division Al of the adductor mandibulae: A OP, ligament; SH. sternohvoideus muscle. FEEDING MECHANISMS IN RAY-FINNED FISHES 277 phasize characteristic features of the Ac- surface of the branchiostegal rays to insert tinopterygii, Halecostomi, Teleostei, Neo- in the fascia dorsal to the intermandibu- teleostei, and Percomorpha with the goal laris posterior. The hyohyoideus muscu- of suggesting certain general propositions lature of halecostomes appears to be de- about the nature of change in structural rived from the interhyoideus muscle fibers and functional networks within lineages of primitive actinopterygians (Fig. 2B: (also see Lauder, 1981). IH). The skull of primitive actinopterygians PRIMITIVE FEATURES OF THE possesses only a few mobile elements (Blot, ACTINOPTERYGIAN FEEDING MECHANISM 1978; Saint-Seine, 1956). The maxilla and Mouth opening in primitive actinopte- premaxilla are firmly attached to the other rygians is mediated by two musculoskeletal dermal skull bones and the opercle, sub- couplings (Figs. 1A, 2): the epaxial mus- opercle, and branchiostegal rays have lim- cles—neurocranium coupling which ele- ited lateral mobility. The oblique angle of vates the head (Fig. 1A: coupling 2), and the suspensory apparatus (reflected by the a ventral coupling involving the hypaxial position of the preoperculum, Fig. 2A: musculature, cleithrum, sternohyoideus, POP), results in a distinctly postorbital jaw and hyoid apparatus (Fig. 1A: coupling 1) articulation and limited lateral expansion. which causes mandibular depression. The three adductor mandibulae divisions Depression of the lower jaw is effected by are contained in a postorbital maxillary- retraction of the hyoid apparatus (by the palatoquadrate chamber. sternohyoideus and obliquus inferioris The experimental study of prey capture muscles) which exerts a posterodorsal in the primitive living actinopterygians Po- force on the mandible via the mandibulo- lypterus and Lepisosteus (Lauder, 1980a; hyoid ligament (Fig. 1A: MHL). This pos- Lauder and Norton, 1980) has revealed terodorsal force is applied at the insertion the importance of synchronous activity in of the mandibulohyoid ligament ventral to the obliquus inferioris and sternohyoideus the quadratomandibular articulation and muscles for mouth opening. The ventral thus causes mandibular depression (also division of the hypaxialis (=obliquus infer- see Lauder, 1980a, Fig. 18; 1980d)- This ioris) stabilizes the pectoral girdle so that mechanism of mandibular depression is the primary effect of the sternohyoideus also found in lungfishes, coelacanths, and is to cause posteroventral hyoid rotation, sharks and is thus primitive for the Tel- thus opening the mouth. Experimental eostomi. analysis reveals no evidence for the pos- A reconstruction of the jaw musculature terior movement of the pectoral girdle in a palaeoniscoid is illustrated in Figure which has been
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